Activity-dependent lateral inhibition enables the synchronization of olfactory bulb projection neurons

Abstract

Information in the brain is represented by the activity of neuronal ensembles. These ensembles are adaptive and dynamic, formed and truncated based on the animal’s experience. One mechanism by which spatially distributed neurons form an ensemble is by synchronizing their spike times in response to a sensory event. In the olfactory bulb, odor stimulation evokes rhythmic gamma activity in spatially distributed mitral and tufted cells (MTCs). This rhythmic activity is thought to enhance the relay of odor information to the downstream olfactory targets. However, how specifically the odor-activated MTCs are synchronized is unknown. Here, we demonstrate that optogenetic activation of one set of MTCs can gamma-entrain the spiking activity of another set. This lateral synchronization was particularly effective when the recorded MTC fired at the gamma rhythm, facilitating the synchronization of only the substantially active MTCs. Furthermore, we show that lateral synchronization did not depend on the distance between the MTCs and is mediated by granule-cell layer neurons. In contrast, lateral inhibition between MTCs that reduced their firing rates was spatially restricted to adjacent MTCs and was not mediated by granule-cell layer neurons. This dissociation between these two interaction types suggests that they are mediated by different neural circuits. Our findings propose a simple yet robust mechanism by which spatially distributed neurons entrain each other spiking activity to form an ensemble.